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CCL28 modulates neutrophil responses during infection with mucosal pathogens

Araceli Perez-Lopez, Steven Silva, Michael H. Lee, Nicholas Dillon, Stephanie L. Brandt, Romana R. Gerner, Karine Melchior, Gregory T. Walker, Victor A. Sosa-Hernandez, Rodrigo Cervantes-Diaz, Sandra Romero-Ramirez, Jose L. Maravillas-Montero, Sean-Paul Nuccio, Victor Nizet, Manuela Raffatellu
doi: https://doi.org/10.1101/2021.03.19.436197
Araceli Perez-Lopez
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
2Department of Microbiology and Molecular Genetics, University of California Irvine, Irvine, CA 92697, USA
3Biomedicine Research Unit, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México. Tlalnepantla, State of México 54090, México
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Steven Silva
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
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Michael H. Lee
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
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Nicholas Dillon
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
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Stephanie L. Brandt
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
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Romana R. Gerner
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
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Karine Melchior
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
4School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, São Paulo, Brazil
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Gregory T. Walker
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
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Victor A. Sosa-Hernandez
5Red de Apoyo a la Investigación, Universidad Nacional Autónoma de México and Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City 14080, México
6Departamento de Biomedicina Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Mexico City 07360, México
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Rodrigo Cervantes-Diaz
5Red de Apoyo a la Investigación, Universidad Nacional Autónoma de México and Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City 14080, México
6Departamento de Biomedicina Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Mexico City 07360, México
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Sandra Romero-Ramirez
5Red de Apoyo a la Investigación, Universidad Nacional Autónoma de México and Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City 14080, México
7Facultad de Medicina, Universidad Nacional Autónoma de México, Mexico City 04510, México
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Jose L. Maravillas-Montero
5Red de Apoyo a la Investigación, Universidad Nacional Autónoma de México and Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City 14080, México
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Sean-Paul Nuccio
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
2Department of Microbiology and Molecular Genetics, University of California Irvine, Irvine, CA 92697, USA
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Victor Nizet
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
8Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA, 92093, USA
9Center for Microbiome Innovation, University of California San Diego, La Jolla, CA 92093, USA
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Manuela Raffatellu
1Division of Host-Microbe Systems & Therapeutics, Department of Pediatrics, University of California San Diego, La Jolla, CA 92093, USA
2Department of Microbiology and Molecular Genetics, University of California Irvine, Irvine, CA 92697, USA
9Center for Microbiome Innovation, University of California San Diego, La Jolla, CA 92093, USA
10Chiba University-UC San Diego Center for Mucosal Immunology, Allergy, and Vaccines (CU-UCSD cMAV), La Jolla, CA 92093, USA
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  • For correspondence: manuelar@ucsd.edu
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Abstract

The chemokine CCL28 is highly expressed in mucosal tissues, but its role during infection is not well understood. Here we show that CCL28 promotes neutrophil accumulation to the gut of mice infected with Salmonella and to the lung of mice infected with Acinetobacter. Neutrophils isolated from the infected mucosa expressed the CCL28 receptors CCR3 and, to a lesser extent, CCR10, on their surface. The functional consequences of CCL28 deficiency were different between the two infections, as Ccl28-/- mice were highly susceptible to Salmonella gut infection, but highly resistant to otherwise lethal Acinetobacter lung infection. In vitro, unstimulated neutrophils harbored pre-formed intracellular CCR3 that was rapidly mobilized to the cell surface following phagocytosis or inflammatory stimuli. Moreover, CCL28 stimulation enhanced neutrophil antimicrobial activity, production of reactive oxygen species, and formation of extracellular traps, all processes that were largely dependent on CCR3. Consistent with the different outcomes in the two infection models, neutrophil stimulation with CCL28 boosted the killing of Salmonella but not of Acinetobacter. CCL28 thus plays a critical role in the immune response to mucosal pathogens by increasing neutrophil accumulation and activation, which can enhance pathogen clearance but also exacerbate disease depending on the mucosal site and the infectious agent.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 09, 2022.
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CCL28 modulates neutrophil responses during infection with mucosal pathogens
Araceli Perez-Lopez, Steven Silva, Michael H. Lee, Nicholas Dillon, Stephanie L. Brandt, Romana R. Gerner, Karine Melchior, Gregory T. Walker, Victor A. Sosa-Hernandez, Rodrigo Cervantes-Diaz, Sandra Romero-Ramirez, Jose L. Maravillas-Montero, Sean-Paul Nuccio, Victor Nizet, Manuela Raffatellu
bioRxiv 2021.03.19.436197; doi: https://doi.org/10.1101/2021.03.19.436197
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CCL28 modulates neutrophil responses during infection with mucosal pathogens
Araceli Perez-Lopez, Steven Silva, Michael H. Lee, Nicholas Dillon, Stephanie L. Brandt, Romana R. Gerner, Karine Melchior, Gregory T. Walker, Victor A. Sosa-Hernandez, Rodrigo Cervantes-Diaz, Sandra Romero-Ramirez, Jose L. Maravillas-Montero, Sean-Paul Nuccio, Victor Nizet, Manuela Raffatellu
bioRxiv 2021.03.19.436197; doi: https://doi.org/10.1101/2021.03.19.436197

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